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Diel pattern of migration in a poisonous toad from Brazil and the evolution of chemical defenses in diurnal amphibians

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Abstract

Most amphibians with biphasic life cycles have aquatic eggs and larvae and terrestrial adults that migrate between terrestrial habitats and aquatic breeding sites. Migration usually occurs at night in order to avoid desiccation and predation. However, some amphibians also migrate during the day, and it has been proposed that this may have evolved as a result of poisonous skin secretions and aposematic coloration that release individuals from visually oriented diurnal predators. Based on this hypothesis and recent observations of 24 h breeding activity in the poisonous, aposematic toad Melanophryniscus cambaraensis, we predicted that migration in this species would occur equally during the day and night. To test our prediction we documented the diel pattern of migratory activity over multiple explosive breeding events from October 2008 to February 2009 (127 nights) at a temporary stream in Rio Grande do Sul state, southern Brazil. We also obtained environmental data to determine if diel activity could be attributed to variation in rainfall, barometric pressure, temperature, and/or relative air humidity. Contrary to our prediction, migratory activity in M. cambaraensis is strongly diurnal. Although temperature and humidity varied significantly between day and night intervals, this variation does not account for the diurnal-only migratory activity of M. cambaraensis. We suggest that the diurnal-only migratory activity of M. cambaraensis is best explained by phylogeny, not contemporary functions or selective pressures. Diurnal activity is primitive for this species and evolved in the common ancestor of Agastorophrynia, prior to the chemical defenses found in toads (Bufonidae) and poison frogs (Dendrobatidae). This suggests that chemical defenses in these groups may have evolved as a result of the diurnal activity that brought them into contact with visually oriented diurnal predators, and not the other way around.

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References

  • Altig R, McDiarmid RW (1999) Body plan. Development and morphology. In: McDiarmid RW, Altig R (eds) Tadpoles. The biology of anuran larvae. The University of Chicago Press, Chicago, pp 24–51

    Google Scholar 

  • Backes A, Felipe L, Viola MG (2005) Produção de serapilheira em Floresta Ombrófila Mista, em São Francisco de Paula, Rio Grande do Sul, Brasil. Acta Bot Bras 19:155–160. doi:10.1590/S0102-33062005000100015

    Article  Google Scholar 

  • Baldo D, Basso NG (2004) A new species of Melanophryniscus Gallardo, 1961 (Anura: Bufonidae), with comments on the species of the genus reported for Misiones, northeastern Argentina. J Herpetol 28:393–403. doi:10.1670/144-03A

    Article  Google Scholar 

  • Bennett AF (1990) Thermal dependence of locomotor capacity. Am J Physiol Regul Integr Comp Physiol 259:R253–R258

    CAS  Google Scholar 

  • Bonatti C, Marczwski M, Rebelato GS et al (2006) Trilhas da Floresta Nacional de São Francisco de Paula, Rio Grande do Sul, Brasil: Mapeamento, análise e estudo da capacidade de carga turística. Rev Bras Biocien 4:15–26

    Google Scholar 

  • Brattstrom BH (1979) Amphibian temperature regulation studies in the field and laboratory. Am Zool 19:345–356

    CAS  Google Scholar 

  • Brodie ED Jr, Formanowicz DR Jr, Brodie ED III (1991) Predator avoidance and antipredator mechanisms: distinct pathways to survival. Ethol Ecol Evol 3:73–77

    Article  Google Scholar 

  • Buriol GA, Estefanel V, Gracioli MSA et al (2009) Climatic zoning of conditions for the development of the larva of the mosquito that transmits the dengue fever virus in the State of Rio Grande do Sul. Elect J Commun Inf Innov Health 3:24–36. doi:10.3395/reciis.v3i2.146en

    Google Scholar 

  • Cade BS, Richards JD (2005) User manual for Blossom statistical software. U.S. Department of Interior, U.S. Geological Survey, Reston, Virginia. Available from http://www.fort.usgs.gov/products/publications/pub_abstract.asp?PubID=21536. Accessed Aug 2008

  • Colombo P, Zank C, Schimidt LEC et al (2007) Anura, Bufonidae, Melanophryniscus simplex: distribution extension. Check List 3:305–307

    Google Scholar 

  • Corn PS (1994) Straight-line drift fences and pitfall traps. In: Heyer WR et al (eds) Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, Washington, pp 109–117

    Google Scholar 

  • Daly JW (2004) Marine toxins and nonmarine toxins: convergence or symbiotic organisms? J Nat Prod 67:1211–1215. doi:10.1021/np040016t

    Article  CAS  PubMed  Google Scholar 

  • Daly JW, Garraffo HM, Spande TF et al (2008) Indolizidine 239Q and quinolizidine 275I. Major alkaloids in two Argentinian bufonid toads (Melanophryniscus). Toxicon 52:858–870. doi:10.1016/j.toxicon.2008.08.016

    Article  CAS  PubMed  Google Scholar 

  • Darst CR, Menéndez-Guerrero PA, Coloma LA, Cannatella DC (2005) Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. Am Nat 165:56–69

    Article  PubMed  Google Scholar 

  • Ferner JW (2007) A review of marking and individual recognition techniques for amphibians and reptiles. Society for the Study of Amphibians and Reptiles, South Lake City

    Google Scholar 

  • Garcia PCA, Vinciprova G (2003) Anfíbios. In: Fontana CS, Bencke GA, Reis RE (eds) Livro vermelho da fauna ameaçada de extinção no Rio Grande do Sul. EDIPUCRS, Porto Alegre, pp 147–164

    Google Scholar 

  • Grant T (2007) A new, toxic species of Colostethus (Anura: Dendrobatidae) from the Cordillera Central of Colombia. Zootaxa 1555:39–51

    Google Scholar 

  • Grant T, Frost DR, Caldwell JP et al (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Anura: Athesphatanura: Dendrobatidae). B Am Mus Nat Hist 299:1–262. doi:10.1206/0003-0090(2006)299[1:PSODFA]2.0.CO;2

    Article  Google Scholar 

  • Hanifin CT (2010) The chemical and evolutionary ecology of tetrodotoxin (TTX) toxicity in terrestrial vertebrates. Mar Drugs 8:577–593. doi:10.3390/md8030577

    Article  CAS  PubMed  Google Scholar 

  • Kwet A, Di-Bernardo M (1999) Anfíbios, amphibien, amphibians. EDIPUCRS, Porto Alegre

    Google Scholar 

  • Kwet A, Maneyro R, Zillikens A et al (2005) Advertisement calls of Melanophryniscus dorsalis (Mertens, 1933) and M. montevidensis (Philippi, 1902), two parapatric species from southern Brazil and Uruguay, with comments on morphological variation in the Melanophryniscus stelzneri group (Anura: Bufonidae). Salamandra 41:1–18

    Google Scholar 

  • Langone JA (1994) Ranas y sapos del Uruguay. Museu Damaso Antonio Larrañaga, Serie de Divulgación, Montevideo

  • Lillywhite HB, Licht P, Chelgren P (1973) The role of behavioral thermoregulation in the growth energetics of the toad, Bufo boreas. Ecology 54:375–383

    Article  Google Scholar 

  • Lötters S (1996) The neotropical toad genus Atelopus. Checklist, biology, distribution. M. Vences & F. Glaw Köln, Germany

    Google Scholar 

  • Maluf JRT (2000) Nova classificação climática do Estado do Rio Grande do Sul. Rev Bras Agromet 8:1–150

    Google Scholar 

  • McDiarmid RW (1971) Comparative morphology and evolution of frogs of the Neotropical genera Atelopus, Dendrophryniscus, Melanophryniscus, and Oreophrynella. Bull Nat Hist Mus Los Angeles Co 12:1–66

    Google Scholar 

  • Navas CA, Gomes FR, Carvalho JE (2008) Thermal relationships and exercise physiology in anuran amphibians: integration and evolutionary implications. Comp Biochem Physiol A 151:344–362

    Article  Google Scholar 

  • Noble GK (1931) The biology of the amphibia. McGraw-Hill, New York

    Google Scholar 

  • Pizzatto L, Child T, Shine R (2008) Why be diurnal? Shifts in activity time enable young cane toads to evade cannibalistic conspecifics. Behav Ecol 19:990–997

    Article  Google Scholar 

  • Rohlf FJ (2000) NTSYS 2.1: numerical taxonomic and multivariate analysis system. Exeter Software, New York

    Google Scholar 

  • Russell AP, Bauer AM, Johnson MK (2005) Migration of amphibians and reptiles: an overview of patterns and orientation mechanisms in relation to life history strategies. In: Elewa MT (ed) Migration of organisms. Springer, Berlin, pp 151–203

    Chapter  Google Scholar 

  • Santos RR, Leonardi SB, Caorsi VZ, Grant T (2010) Directional orientation of migration in an aseasonal explosive-breeding toad from Brazil. J Trop Ecol 26:415–421. doi:10.1017/S0266467410000180

    Article  Google Scholar 

  • Semlitsch RD (1985) Analysis of climatic factors influencing migrations of the salamander Ambystoma talpoideum. Copeia 1985:477–489. doi:10.2307/1444862

    Article  Google Scholar 

  • Semlitsch RD (2008) Differentiating migration and dispersal processes for pond-breeding amphibians. J Wildl Manage 72:260–267. doi:10.2193/2007-082

    Article  Google Scholar 

  • Semlitsch RD, Pechmann JHK (1985) Diel pattern of migratory activity for several species of pond-breeding salamanders. Copeia 1985:86–91. doi:10.2307/1444794

    Article  Google Scholar 

  • Sinsch U (1988) Seasonal changes in the migratory behavior of the toad Bufo bufo: direction and magnitude of movements. Oecologia 76:390–398. doi:10.1007/BF00377034

    Google Scholar 

  • Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632

    Article  Google Scholar 

  • Sonego RC, Backes A, Souza AF (2007) Descrição da estrutura de uma floresta ombrófila mista, RS, Brasil, utilizando estimadores não-paramétricos de riqueza e rarefação de amostras. Acta Bot Bras 21:943–955. doi:10.1590/S0102-33062007000400019

    Article  Google Scholar 

  • Todd BD, Winne CT (2006) Ontogenetic and interspecific variation in timing of movement and responses to climatic factors during migrations by pond-breeding amphibians. Can J Zool 84:715–722. doi:10.1139/Z06-054

    Article  Google Scholar 

  • Wells KD (1977) The social behavior of anuran amphibians. Anim Behav 25:666–693. doi:10.1016/0003-3472(77)90118-X

    Article  Google Scholar 

  • Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, Chicago

    Google Scholar 

Download references

Acknowledgments

Fieldwork was authorized by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis under license number 17288-1 and was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Procs. 305473/2008-5 and 476789/2009-5 and a Master’s fellowship to RRS) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Proc. 2008/50928-1). Weather data were provided by the Brazilian Instituto Nacional de Meteorologia. We are grateful to Patrick Colombo and Ralph Saporito for advice on the design and implementation of this study and Camila Both and Clarissa Britz for guidance on data analysis. Edenice Brandão Ávila de Souza and the personnel at the Floresta Nacional de São Francisco de Paula supported all aspects of our fieldwork. We thank Camila Both, Patrick Colombo, Célio Haddad, Márcio Martins, Tracy Rittenhouse, Ralph Saporito and anonymous reviewers for critically reading the manuscript. Finally, we express our gratitude to the many colleagues who helped install traps and collect data.

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  1. Pontifícia Universidade Católica do Rio Grande do Sul, Faculdade de Biociências, Avenida Ipiranga 6681, 90619-900, Porto Alegre, RS, Brazil

    Raquel Rocha Santos & Taran Grant

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  1. Raquel Rocha Santos
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  2. Taran Grant
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Correspondence to Taran Grant.

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Santos, R.R., Grant, T. Diel pattern of migration in a poisonous toad from Brazil and the evolution of chemical defenses in diurnal amphibians. Evol Ecol 25, 249–258 (2011). https://doi.org/10.1007/s10682-010-9407-0

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